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Fungal Infection Induces Sex-Specific Transcriptional Changes and Alters Sexual Dimorphism in the Dioecious Plant


Females and males differ from each other in many traits, including morphology, behavior and physiology. Differences in gene expression between the sexes, known as sex-biased gene expression, contribute to such sexual dimorphism. Here we characterize the responses of females and males of the dioecious plant Silene latifolia to infection with the anther smut fungus Micobrotryum lychnidis-dioicae. This fungus sterilizes the plant and induces a partial sex reversal in female hosts that form rudimentary stamens, thus allowing the fungus to transmit its spores via pollinators. Our comparisons of gene expression in healthy and infected plants reveal strong sex-specific responses to anther smut infection. Expression changes in females and males are in opposite directions and are associated with reduced sexual dimorphism between infected females and males. Our study reveals that infection with the anther smut fungus alters the extent of sex-biased gene expression in S. latifolia in a sex-specific manner and highlights how transcriptomic changes in females and males shape sexual dimorphism.


Vyšlo v časopise: Fungal Infection Induces Sex-Specific Transcriptional Changes and Alters Sexual Dimorphism in the Dioecious Plant. PLoS Genet 11(10): e32767. doi:10.1371/journal.pgen.1005536
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005536

Souhrn

Females and males differ from each other in many traits, including morphology, behavior and physiology. Differences in gene expression between the sexes, known as sex-biased gene expression, contribute to such sexual dimorphism. Here we characterize the responses of females and males of the dioecious plant Silene latifolia to infection with the anther smut fungus Micobrotryum lychnidis-dioicae. This fungus sterilizes the plant and induces a partial sex reversal in female hosts that form rudimentary stamens, thus allowing the fungus to transmit its spores via pollinators. Our comparisons of gene expression in healthy and infected plants reveal strong sex-specific responses to anther smut infection. Expression changes in females and males are in opposite directions and are associated with reduced sexual dimorphism between infected females and males. Our study reveals that infection with the anther smut fungus alters the extent of sex-biased gene expression in S. latifolia in a sex-specific manner and highlights how transcriptomic changes in females and males shape sexual dimorphism.


Zdroje

1. Ellegren H, Parsch J (2007) The evolution of sex-biased genes and sex-biased gene expression. Nat Rev Genet 8: 689–698. 17680007

2. Mank JE (2009) Sex chromosomes and the evolution of sexual dimorphism: Lessons from the genome. Am Nat 173: 141–150. doi: 10.1086/595754 20374139

3. Rice WR (1984) Sex-chromosomes and the evolution of sexual dimorphism. Evolution 38: 735–742.

4. Innocenti P, Morrow EH (2010) The sexually antagonistic genes of Drosophila melanogaster. Plos Biol 8.

5. Yang X, Schadt EE, Wang S, Wang H, Arnold AP, et al. (2006) Tissue-specific expression and regulation of sexually dimorphic genes in mice. Genome Res 16: 995–1004. 16825664

6. Kang HJ, Kawasawa YI, Cheng F, Zhu Y, Xu XM, et al. (2011) Spatio-temporal transcriptome of the human brain. Nature 478: 483–489. doi: 10.1038/nature10523 22031440

7. Duneau D, Ebert D (2012) Host sexual dimorphism and parasite adaptation. Plos Biol 10: e1001271. doi: 10.1371/journal.pbio.1001271 22389630

8. Zuk M, McKean KA (1996) Sex differences in parasite infections: Patterns and processes. Int J Parasitol 26: 1009–1023. 8982783

9. Yeretssian G, Doiron K, Shao W, Leavitt BR, Hayden MR, et al. (2009) Gender differences in expression of the human caspase-12 long variant determines susceptibility to Listeria monocytogenes infection. P Natl Acad Sci USA 106: 9016–9020.

10. Xiao J, Kannan G, Jones-Brando L, Brannock C, Krasnova IN, et al. (2012) Sex-specific changes in gene expression and behavior induced by chronic toxoplasma infection in mice. Neuroscience 206: 39–48. doi: 10.1016/j.neuroscience.2011.12.051 22240252

11. Slansky F (2007) Insect/Mammal associations: Effects of cuterebrid bot fly parasites on their hosts. Annu Rev Entomol 52: 17–36. 16972767

12. van Houte S, Ros VID, van Oers MM (2013) Walking with insects: molecular mechanisms behind parasitic manipulation of host behaviour. Mol Ecol 22: 3458–3475. doi: 10.1111/mec.12307 23742168

13. Engelstadter J, Hurst GDD (2009) The ecology and evolution of microbes that manipulate host R&Deproduction. Annu Rev Ecol Evol S 40: 127–149.

14. Rodgers-Gray TP, Smith JE, Ashcroft AE, Isaac RE, Dunn AM (2004) Mechanisms of parasite-induced sex reversal in Gammarus duebeni. Int J Parasitol 34: 747–753. 15111096

15. Antonovics J (2005) Plant venereal diseases: insights from a messy metaphor. New Phytol 165: 71–80. 15720622

16. Bernasconi G, Antonovics J, Biere A, Charlesworth D, Delph LF, et al. (2009) Silene as a model system in ecology and evolution. Heredity 103: 5–14. doi: 10.1038/hdy.2009.34 19367316

17. Nicolas M, Marais G, Hykelova V, Janousek B, Laporte V, et al. (2005) A gradual process of recombination restriction in the evolutionary history of the sex chromosomes in dioecious plants. Plos Biol 3: 47–56.

18. Marais GAB, Nicolas M, Bergero R, Chambrier P, Kejnovsky E, et al. (2008) Evidence for degeneration of the Y chromosome in the dioecious plant Silene latifolia. Curr Biol 18: 545–549. doi: 10.1016/j.cub.2008.03.023 18394889

19. Muyle A, Zemp N, Deschamps C, Mousset S, Widmer A, et al. (2012) Rapid de novo evolution of X chromosome dosage compensation in Silene latifolia, a plant with young sex chromosomes. Plos Biol 10: e1001308. doi: 10.1371/journal.pbio.1001308 22529744

20. Bergero R, Charlesworth D (2011) Preservation of the Y transcriptome in a 10-million-year-old plant sex chromosome system. Curr Biol 21: 1470–1474. doi: 10.1016/j.cub.2011.07.032 21889891

21. Chibalina MV, Filatov DA (2011) Plant Y chromosome degeneration is retarded by haploid purifying selection. Curr Biol 21: 1475–1479. doi: 10.1016/j.cub.2011.07.045 21889890

22. Bergero R, Charlesworth D (2011) Preservation of the Y transcriptome in a 10-million-year-old plant sex chromosome system. Curr Biol 21: 1470–1474. doi: 10.1016/j.cub.2011.07.032 21889891

23. Bergero R, Qiu S, Charlesworth D (2015) Gene loss from a plant dex chromosome system. Curr Biol 25: 1234–1240. doi: 10.1016/j.cub.2015.03.015 25913399

24. Chibalina MV, Filatov DA (2011) Plant Y chromosome degeneration is retarded by haploid purifying selection. Curr Biol 21: 1475–1479. doi: 10.1016/j.cub.2011.07.045 21889890

25. Delph LF, Arntz AM, Scotti-Saintagne C, Scotti I (2010) The genomic architecture of sexual dimorphism in the dioecious plant Silene latifolia. Evolution 64: 2873–2886. doi: 10.1111/j.1558-5646.2010.01048.x 20550575

26. Le Gac M, Hood ME, Fournier E, Giraud T (2007) Phylogenetic evidence of host-specific cryptic species in the anther smut fungus. Evolution 61: 15–26. 17300424

27. Baker HG (1947) Infection of species of Melandrium by Ustilago violacea (Pers) Fuckel and the transmission of the resultant disease. Ann Bot-London 11: 333–348.

28. Refregier G, Le Gac M, Jabbour F, Widmer A, Shykoff JA, et al. (2008) Cophylogeny of the anther smut fungi and their caryophyllaceous hosts: Prevalence of host shifts and importance of delimiting parasite species for inferring cospeciation. Bmc Evol Biol 8.

29. Sloan DB, Giraud T, Hood ME (2008) Maximized virulence in a sterilizing pathogen: the anther-smut fungus and its co-evolved hosts. J Evolution Biol 21: 1544–1554.

30. Hood ME, Mena-Alí JI, Gibson AK, Oxelman B, Giraud T, et al. (2010) Distribution of the anther-smut pathogen Microbotryum on species of the Caryophyllaceae. New Phytol 187: 217–229. doi: 10.1111/j.1469-8137.2010.03268.x 20406409

31. Kazama Y, Koizumi A, Uchida W, Ageez A, Kawano S (2005) Expression of the floral B-function gene SLM2 in female flowers of Silene latifolia infected with the smut fungus Microbotryum violaceum. Plant and Cell Physiology 46: 806–811. 15755743

32. Ageez A, Kazama Y, Sugiyama R, Kawano S (2005) Male-fertility genes expressed in male flower buds of Silene latifolia include homologs of anther-specific genes. Genes & Genetic Systems 80: 403–413.16501309

33. Scutt CP, Li Y, Robertson SE, Willis ME, Gilmartin PM (1997) Sex determination in dioecious Silene latifolia—Effects of the Y chromosome and the parasitic smut fungus (Ustilago violacea) on gene expression during flower development. Plant Physiology 114: 969–979. 9232878

34. Westermann AJ, Gorski SA, Vogel J (2012) Dual RNA-seq of pathogen and host. Nat Rev Microbiol 10: 618–630. doi: 10.1038/nrmicro2852 22890146

35. Marriott I, Huet-Hudson YM (2006) Sexual dimorphism in innate immune responses to infectious organisms. Immunol Res 34: 177–192. 16891670

36. Wise RP, Moscou MJ, Bogdanove AJ, Whitham SA (2007) Transcript profiling in host-pathogen interactions. Annu Rev Phytopathol 45: 329–369. 17480183

37. Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet 11: 539–548. doi: 10.1038/nrg2812 20585331

38. Fuller VL, Lilley CJ, Atkinson HJ, Urwin PE (2007) Differential gene expression in Arabidopsis following infection by plant-parasitic nematodes Meloidogyne incognita and Heterodera schachtii. Mol Plant Pathol 8: 595–609. doi: 10.1111/j.1364-3703.2007.00416.x 20507524

39. Kyndt T, Denil S, Haegeman A, Trooskens G, Bauters L, et al. (2012) Transcriptional reprogramming by root knot and migratory nematode infection in rice. New Phytol 196: 887–900. doi: 10.1111/j.1469-8137.2012.04311.x 22985291

40. Jenner RG, Young RA (2005) Insights into host responses against pathogens from transcriptional profiling. Nat Rev Microbiol 3: 281–294. 15806094

41. Biere A, Honders SC (1998) Anther smut transmission in Silene latifolia and Silene dioica: Impact of host traits, disease frequency, and host density. Int J Plant Sci 159: 228–235.

42. Thrall PH, Jarosz AM (1994) Host-pathogen dynamics in experimental populations of Silene alba and Ustilago violacea. I. ecological and genetic determinants of disease spread. J Ecol 82: 549–559.

43. Waelti MO, Page PA, Widmer A, Schiestl FP (2009) How to be an attractive male: floral dimorphism and attractiveness to pollinators in a dioecious plant. Bmc Evol Biol 9.

44. Barrett SCH, Hough J (2013) Sexual dimorphism in flowering plants. J Exp Bot 64: 67–82. doi: 10.1093/jxb/ers308 23183260

45. Kaltz O, Shykoff JA (2001) Male and female Silene latifolia plants differ in per-contact risk of infection by a sexually transmitted disease. J Ecol 89: 99–109.

46. Kumar S, Hedges SB (2011) TimeTree2: species divergence times on the iPhone. Bioinformatics 27: 2023–2024. doi: 10.1093/bioinformatics/btr315 21622662

47. Primmer CR, Papakostas S, Leder EH, Davis MJ, Ragan MA (2013) Annotated genes and nonannotated genomes: cross-species use of Gene Ontology in ecology and evolution research. Mol Ecol 22: 3216–3241. doi: 10.1111/mec.12309 23763602

48. Lodha TD, Basak J (2012) Plant-pathogen interactions: what microarray tells about it? Molecular biotechnology 50: 87–97. doi: 10.1007/s12033-011-9418-2 21618071

49. Locklin JL, Vodopich DS (2010) Patterns of gregarine parasitism in dragonflies: host, habitat, and seasonality. Parasitol Res 107: 75–87. doi: 10.1007/s00436-010-1836-8 20376487

50. Duneau D, Luijckx P, Ruder LF, Ebert D (2012) Sex-specific effects of a parasite evolving in a female-biased host population. Bmc Biol 10.

51. Shykoff JA, Kaltz O (1997) Effects of the anther smut fungus Microbotryum violaceum on host life-history patterns in Silene latifolia (Caryophyllaceae). Int J Plant Sci 158: 164–171.

52. Shykoff JA, Kaltz O (1998) Phenotypic changes in host plants diseased by Microbotryum violaceum: Parasite manipulation, side effects, and trade-offs. Int J Plant Sci 159: 236–243.

53. Uchida W, Matsunaga S, Sugiyama R, Kazama Y, Kawano S (2003) Morphological development of anthers induced by the dimorphic smut fungus Microbotryum violaceum in female flowers of the dioecious plant Silene latifolia. Planta 218: 240–248. 14551772

54. Carpenter J, Hutter S, Baines JF, Roller J, Saminadin-Peter SS, et al. (2009) The Transcriptional Response of Drosophila melanogaster to Infection with the Sigma Virus (Rhabdoviridae). Plos One 4.

55. Martin A, Troadec C, Boualem A, Rajab M, Fernandez R, et al. (2009) A transposon-induced epigenetic change leads to sex determination in melon. Nature 461: 1135–U1237. doi: 10.1038/nature08498 19847267

56. Charlesworth D, Morgan MT (1991) Allocation of resources to sex functions in flowering plants. Philos T R Soc B 332: 91–102.

57. Pointer MA, Harrison PW, Wright AE, Mank JE (2013) Masculinization of gene expression is associated with exaggeration of male sexual dimorphism. Plos Genet 9: e1003697. doi: 10.1371/journal.pgen.1003697 23966876

58. Alexander HM, Maltby A (1990) Anther-smut infection of Silene alba caused by Ustilago violacea—Factors determining fungal reproduction. Oecologia 84: 249–253.

59. Grant S, Hunkirchen B, Saedler H (1994) Developmental differences between male and female flowers in the dioecious plant Silene latifolia. Plant J 6: 471–480.

60. Zemp N, Minder A, Widmer A (2014) Identification of internal reference genes for gene expression normalization between the two sexes in dioecious White Campion. Plos One 9: e92893. doi: 10.1371/journal.pone.0092893 24675788

61. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754–1760. doi: 10.1093/bioinformatics/btp324 19451168

62. Macas J, Kejnovsky E, Neumann P, Novák P, Koblížková A, et al. (2011) Next generation sequencing-based analysis of repetitive DNA in the model dioceous plant Silene latifolia. Plos One 6: e27335. doi: 10.1371/journal.pone.0027335 22096552

63. Smit A, Hubley R, Green P (1996–2010) RepeatMasker Open-3.0. http://www.repeatmasker.org.

64. Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139–140. doi: 10.1093/bioinformatics/btp616 19910308

65. R Development Core Team (2012) R: A language and environment for statistical computing, reference index version 2.15.0. R Foundation for Statistical Computing, Vienna, Austria.

66. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, et al. (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674–3676. 16081474

67. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nature methods 9: 671–675. 22930834

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